Balancing selection and the crossing of fitness valleys in structured populations: diversification in the gametophytic self-incompatibility system

The self-incompatibility locus (S-locus) of flowering plants displays a striking allelic diversity. How such a diversity has emerged remains unclear. In this paper, we performed numerical simulations in a finite island population genetics model to investigate how population subdivision affects the diversification process at a S-locus, given that the two-genes architecture typical of S-loci involves the crossing of a fitness valley. We show that population structure increases the number of self-incompatibility haplotypes (S-haplotypes) maintained in the whole metapopulation, but at the same time also slightly reduces the parameter range allowing for their diversification. This increase is partly due to a reinforcement of the diversification and replacement dynamics of S-haplotypes within and among demes. We also show that the two-genes architecture leads to a higher diversity compared with a simpler genetic architecture where new S-haplotypes appear in a single mutation step. We conclude that population structure helps explain the large allelic diversity at the self-incompatibility locus. Overall, our results suggest that population subdivision can act in two opposite directions: it makes easier S-haplotypes diversification but increases the risk that the SI system is lost.

Perennial Rye: Genetics of Perenniality and Limited Fertility

Perenniality, the ability of plants to regrow after seed set, could be introgressed into cultivated rye by crossing with the wild relative and perennial Secale strictum. However, studies in the past showed that Secale cereale × Secale strictum-derived cultivars were also characterized by reduced fertility what was related to so called chromosomal multivalents, bulks of chromosomes that paired together in metaphase I of pollen mother cells instead of only two chromosomes (bivalents). Those multivalents could be caused by ancient translocations that occurred between both species. Genetic studies on perennial rye are quite old and especially the advent of molecular markers and genome sequencing paved the way for new insights and more comprehensive studies. After a brief review of the past research, we used a basic QTL mapping approach to analyze the genetic status of perennial rye. We could show that for the trait perennation 0.74 of the genetic variance in our population was explained by additively inherited QTLs on chromosome 2R, 3R, 4R, 5R and 7R. Fertility on the other hand was with 0.64 of explained genetic variance mainly attributed to a locus on chromosome 5R, what was most probably the self-incompatibility locus S5. Additionally, we could trace the Z locus on chromosome 2R by high segregation distortion of markers. Indications for chromosomal co-segregation, like multivalents, could not be found. This study opens new possibilities to use perennial rye as genetic resource and for alternative breeding methods, as well as a valuable resource for comparative studies of perennation across different species.

Diversification or collapse of self-incompatibility haplotypes as a rescue process

In angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges limit the spread of a new allele (a tightly linked haplotype in this case) under the widespread “collaborative non-self recognition” mechanism. First, there is no obvious selective benefit for pollen compatible with non-existent stylar incompatibilities, which themselves cannot spread if no pollen can fertilize them. However, a pistil-function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. Second, we show that novel haplotypes can drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10–40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.

Diversification or collapse of self-incompatibility haplotypes as outcomes of evolutionary rescue

Self-incompatibility systems in angiosperms are exemplars of extreme allelic polymorphism maintained by long-term balancing selection. Pollen that shares an allele with the pollen recipient at the self-incompatibility locus is rejected, and this rejection favors rare alleles as well as preventing self-fertilization. Advances in molecular genetics reveal that an ancient, deeply conserved, and well-studied incompatibility system functions through multiple tightly linked genes encoding separate pollen-expressed F-box proteins and pistil-expressed ribonucleases. We show that certain recombinant haplotypes at the incompatibility locus can drive collapse in the number of incompatibility types. We use a modified evolutionary rescue model to calculate the relative probabilities of increase and collapse in number of incompatibility types given the initial collection of incompatibility haplotypes and the population rate of gene conversion. We find that expansion in haplotype number is possible when population size or the rate of gene conversion is large, but large contractions are likely otherwise. By iterating a Markov chain model derived from these expansion and collapse probabilities, we find that a stable haplotype number distribution in the realistic range of 10–40 is possible under plausible parameters. However, small or moderate-sized populations should be susceptible to substantial additional loss of haplotypes beyond those lost by chance during bottlenecks. The same processes that can generate many incompatibility haplotypes in large populations may therefore be crushing haplotype diversity in smaller populations.

A triple-hybrid cross reveals a new hybrid incompatibility locus between D. melanogaster and D. sechellia

Hybrid incompatibilities are the result of deleterious interactions between diverged genes in the progeny of two species. In Drosophila, crosses between female D. melanogaster and males from the D. simulans clade (D. simulans, D. mauritiana, D. sechellia) fail to produce hybrid F1 males. When attempting to rescue hybrid F1 males by depleting the incompatible allele of a previously identified hybrid incompatibility gene, we observed robust rescue in crosses of D. melanogaster to D. simulans or D. mauritiana, but no rescue in crosses to D. sechellia. To investigate the genetic basis of D. sechellia resistance to hybrid rescue, we designed a triple-hybrid cross to generate recombinant D. sechellia / D. simulans genotypes. We tested the ability of those genotypes to rescue hybrid males with D. melanogaster, and used whole genome sequencing to measure the D. sechellia / D. simulans allele frequency of viable F1 males. We found that recombinant genotypes were rescued when they contained two specific loci from D. simulans – a region containing previously identified Lethal hybrid rescue (Lhr), and an unknown region of chromosome 3L which we name Sechellia aversion to hybrid rescue (Satyr). Our results show that the genetic basis for the recent evolution of this hybrid incompatibility is simple rather than a highly dispersed effect. Further, these data suggest that fixation of differences at Lhr after the split of the D. simulans clade strengthened the hybrid incompatibility between D. sechellia and D. melanogaster.